Skip to main content
Log in

Identification and characterization of a novel miR159 target not related to MYB in tomato

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

MicroRNA 159 (miR159) is a highly conserved miRNA with roles in flowering under short days, anther development and seed germination via repression of GAMYB-like genes. In tomato, the function of miR159 (Sl-miR159) is currently unknown and target transcripts have not been experimentally validated. Here, we identified and characterized a new miR159 target gene (SGN-U567133) in Solanum lycopersicum (tomato) that is not related to MYB. SGN-U567133 is predominantly expressed in flowers and encodes a nuclear-localized protein that contains a unique NOZZLE-like domain at its N terminus. In tomato, SGN-U567133 represents a small gene family and orthologs have been identified in other plant species, all containing a conserved miR159 target site in their coding sequence. Accordingly, 5′-RACE cleavage assay supported miRNA-mediated cleavage of SGN-U567133 transcripts in vivo. Moreover, the SGN-U567133 transcript accumulated in P19-HA-expressing tomato leaves in which miRNA-mediated cleavage is inhibited. In addition, transgenic tomato plants expressing a miR159-resistant form of SGN-U567133 accumulated higher levels of the SGN-U567133 transcript and exhibited defects in leaf and flower development. Together, our results suggest that SGN-U567133 represents a novel class of miR159 targets in plants and raise the possibility that its post-transcriptional regulation by Sl-miR159 is essential for normal tomato development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

miR159:

MicroRNA 159

miRNA:

Micro RNA

Tomato:

Solanum lycopersicum

References

  • Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365

    Article  CAS  PubMed  Google Scholar 

  • Allen RS, Li J, Stahle MI, Dubroue A, Gubler F, Millar AA (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc Natl Acad Sci USA 104:16371–16376

    Article  CAS  PubMed  Google Scholar 

  • Arazi T, Talmor-Neiman M, Stav R, Riese M, Huijser P, Baulcombe DC (2005) Cloning and characterization of micro-RNAs from moss. Plant J 43:837–848

    Article  CAS  PubMed  Google Scholar 

  • Axtell MJ, Bowman JL (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci 13:343–349

    Article  CAS  PubMed  Google Scholar 

  • Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769

    Article  CAS  PubMed  Google Scholar 

  • Balasubramanian S, Schneitz K (2000) NOZZLE regulates proximal–distal pattern formation, cell proliferation and early sporogenesis during ovule development in Arabidopsis thaliana. Development 127:4227–4238

    CAS  PubMed  Google Scholar 

  • Balasubramanian S, Schneitz K (2002) NOZZLE links proximal–distal and adaxial–abaxial pattern formation during ovule development in Arabidopsis thaliana. Development 129:4291–4300

    CAS  PubMed  Google Scholar 

  • Barg R, Pilowsky M, Shabtai S, Carmi N, Szechtman AD, Dedicova B, Salts Y (1997) The TYLCV-tolerant tomato line MP-1 is characterized by superior transformation competence. J Exp Bot 48:1919–1923

    CAS  Google Scholar 

  • Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102:11928–11933

    Article  CAS  PubMed  Google Scholar 

  • Beauclair L, Yu A, Bouche N (2010) microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J 62:454–462

    Article  CAS  PubMed  Google Scholar 

  • Berger Y, Harpaz-Saad S, Brand A, Melnik H, Sirding N, Alvarez JP, Zinder M, Samach A, Eshed Y, Ori N (2009) The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136:823–832

    Article  CAS  PubMed  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Fahlgren N, Carrington JC (2010) miRNA target prediction in plants. Humana Press, Clifton

    Google Scholar 

  • Gandikota M, Birkenbihl RP, Hohmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693

    Article  CAS  PubMed  Google Scholar 

  • Garcia D (2008) A miRacle in plant development: role of microRNAs in cell differentiation and patterning. Semin Cell Dev Biol 19:586–595

    Article  CAS  PubMed  Google Scholar 

  • Gong X, Bewley DJ (2008) A GAMYB-like gene in tomato and its expression during seed germination. Planta 228:563–572

    Article  CAS  PubMed  Google Scholar 

  • Griffiths-Jones S (2004) The microRNA registry. Nucleic Acids Res 32(Database issue):D109–D111

    Article  CAS  PubMed  Google Scholar 

  • Gubler F, Kalla R, Roberts JK, Jacobsen JV (1995) Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. Plant Cell 7:1879–1891

    Article  CAS  PubMed  Google Scholar 

  • Gubler F, Raventos D, Keys M, Watts R, Mundy J, Jacobsen JV (1999) Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J 17:1–9

    Article  CAS  PubMed  Google Scholar 

  • Helliwell C, Waterhouse P (2003) Constructs and methods for high-throughput gene silencing in plants. Methods 30:289–295

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    Article  PubMed  Google Scholar 

  • Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann JL, Meyerowitz EM (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430:356–360

    Article  CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    Article  CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  CAS  PubMed  Google Scholar 

  • Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M, Matsuoka M (2004) Loss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development. Plant Cell 16:33–44

    Article  CAS  PubMed  Google Scholar 

  • Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321

    Article  CAS  PubMed  Google Scholar 

  • Lee JH, Cho YS, Yoon HS, Suh MC, Moon J, Lee I, Weigel D, Yun CH, Kim JK (2005) Conservation and divergence of FCA function between Arabidopsis and rice. Plant Mol Biol 58:823–838

    Article  CAS  PubMed  Google Scholar 

  • Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    Article  CAS  PubMed  Google Scholar 

  • Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love K, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89:737–745

    Article  CAS  PubMed  Google Scholar 

  • Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17:705–721

    Article  CAS  PubMed  Google Scholar 

  • Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, Menda N, Amsellem Z, Efroni I, Pekker I, Alvarez JP, Blum E, Zamir D, Eshed Y (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39:787–791

    Article  CAS  PubMed  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  CAS  PubMed  Google Scholar 

  • Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, Rodriguez R, Warthmann N, Allen E, Dezulian T, Huson D, Carrington JC, Weigel D (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13:115–125

    Article  CAS  PubMed  Google Scholar 

  • Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10:1507–1517

    Article  CAS  PubMed  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    Article  CAS  PubMed  Google Scholar 

  • Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49:592–606

    Article  CAS  PubMed  Google Scholar 

  • Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15:244–248

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:11664–11669

    Article  CAS  PubMed  Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527

    Article  CAS  PubMed  Google Scholar 

  • Stav R, Hendelman A, Buxdorf K, Arazi T (2010) Transgenic expression of tomato bushy stunt virus silencing suppressor P19 via the pOp/LhG4 transactivation system induces viral-like symptoms in tomato. Virus Genes 40:119–129

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309

    Article  CAS  PubMed  Google Scholar 

  • Talmor-Neiman M, Stav R, Klipcan L, Buxdorf K, Baulcombe DC, Arazi T (2006) Identification of trans-acting siRNAs in moss and an RNA-dependent RNA polymerase required for their biogenesis. Plant J 48:511–521

    Article  CAS  PubMed  Google Scholar 

  • Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17:49–63

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R, Nishizawa NK, Gomi K, Shimada A, Kitano H, Ashikari M, Matsuoka M (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47:427–444

    Article  CAS  PubMed  Google Scholar 

  • Yang WC, Ye D, Xu J, Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev 13:2108–2117

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Zeng R, Chen J, Liu X, Liao Q (2008) Identification of conserved microRNAs and their targets from Solanum lycopersicum Mill. Gene 423:1–7

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the BARD grant IS-4033-07 and by a grant from the Chief Scientist of the Israel Ministry of Agriculture and Rural Development number: 256-0690-05 to T.A. This is contribution no. 120/2010 series from the Agricultural Research Organization, the Volcani Center, Israel.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tzahi Arazi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 300 kb)

Supplementary material 2 (PDF 109 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buxdorf, K., Hendelman, A., Stav, R. et al. Identification and characterization of a novel miR159 target not related to MYB in tomato. Planta 232, 1009–1022 (2010). https://doi.org/10.1007/s00425-010-1231-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1231-9

Keywords

Navigation